Spread of soybean cyst nematode Heterodera glycines (SCN) to much of
the soybean (Glycine max) growing region in the Midwest has created a
persistent and significant annual yield loss for soybean. Host resistance has
been the primary means of reducing yield loss to SCN. It is not known how
moderately resistant cultivars fit into the management of SCN. Moderately
resistant cultivars can have high yield potential, but nematode reproduction is
greater than on resistant cultivars. Moderate resistance is defined by a SCN
female index (FI) of 10 to 29 in standardized tests, whereas cultivars with an
FI < 10 are considered resistant. Two each of SCN-resistant, moderately
resistant, and susceptible (FI > 60) cultivars were planted in the same plots
for two soybean crops in annual rotation with corn. The SCN population was
reduced 80 and 54% by resistant and moderately resistant cultivars,
respectively, and increased 189% by the susceptible. Yields of the resistant and
moderately resistant were 8.2 and 11.8 bu/acre better, respectively, than for the
susceptible. All plots were planted to a susceptible cultivar in the final year
of the study, and demonstrated there was a carry-over effect from previous
cultivars. Following resistant and moderately resistant cultivars, yields of the
susceptible were 6.6 and 4.3 bu/acre above following susceptible cultivars. This
study showed that moderately resistant soybean cultivars can be an effective
tool for improving profitability of soybean.

Introduction

Soybean cyst nematode (SCN), Heterodera glycines, has spread to much
of the soybean (Glycine max) growing region in the Midwest. A survey in
Illinois found 83% of the fields infested with SCN (7). Yield losses up to 30%
have been reported, which do not always correlate well with population densities
of SCN, because losses are also influenced by other factors such as soil type,
cultivar, and environment (3); however, reducing population densities of SCN has
been a major component of managing SCN.

Host resistance has been one of the main tools utilized to reduce yield loss
to SCN through increased yield and reduced SCN population density (2).
Lengthening the time between the planting of SCN-susceptible hosts through crop
rotation has been another successful tool for reducing the yield loss to SCN
(5). However, in much of the northern soybean growing region of the United
States, soybean is grown in annual rotation with corn, resulting in heavy
reliance upon resistant cultivars to improve yields in the presence of SCN (2).

Many cultivars labeled as resistant do not perform equally, either in terms
of yield or reducing SCN reproduction. Initially, lower yield potential,
commonly know as yield drag, was associated with SCN resistance, but the yield
potential of resistant cultivars has improved. As a result, many of the top
cultivars in yield trials have been those labeled as SCN-resistant (4)
Additionally, testing at the University of Illinois has shown that there is a
high level of variability among cultivars labeled "resistant" in terms of
nematode reproduction (9). The classical definition of SCN resistance (8) is
based on SCN development, measured as a female index (FI) (6). The FI is the
mean number of females produced on a soybean cultivar, divided by the mean
number of females on a susceptible check cultivar, × 100, in a standardized
test. A cultivar with an FI < 10 is SCN-resistant (R); cultivars with FI 10 to
29 are moderately resistant (MR); those with FI 30 to 60 are moderately
susceptible (MS); and those with FI > 60 are susceptible (s). Yield trial
results have shown some MR cultivars can have very good yield potential. The
goals of this research were to: (i) compare the effects of a set of R, MR, and S
soybean cultivars on the population dynamics of SCN in a naturally-infested
field through two soybean crops in an annual rotation of corn/soybean; (ii)
compare the yields of these cultivars; and (iii) determine if the use of resistant
cultivars in previous years may have benefits for subsequent soybean crops
through reduction in SCN population density.

Field Comparison of Moderately Resistant Cultivars

The experimental design was a randomized complete block with six
replications, planted at the University of Illinois Northwestern Illinois
Agricultural Research and Demonstration Center (NWRC) at Monmouth, Illinois. Two
fields were used, designated F4 and E1. The soil types were Muscatune silt loam
(2% sand, 73% silt, 25% clay, 4 to 6% organic matter) and Sable silty clay loam (2% sand, 67%
silt, 31% clay, 4 to 6% organic matter). Six soybean cultivars, two each labeled susceptible
(S), moderately resistant (MR), and resistant (R) to SCN, were planted
individually in 50-ft-long by 20-ft-wide plots, with 8 rows of 30-inch spacing.
The cultivars planted in 2001 and 2002 were 9306 (S), 93B82 (S), 93B11 (MR),
93B66 (MR), 92B91 (R), and 93B67 (R). Due to seed availability issues in 2003
and 2004 the following cultivars were replaced, 9306 replaced with 92B84 (S),
93B11 replaced with 93B15 (MR), and 93B66 replaced with 93B86 (MR). Planting
dates for the study were 16 May for 2001 and 2003, and 10 May for 2002 and 2004.
All cultivars were provided by Pioneer Hi-Bred International, and ranged in
maturity from 2.8 to 3.8. Resistance labeling by Pioneer was as follows: "R" if
their isolate of SCN ‘Race 3’ produced FI of 8 to 15, and "MR" for FI of 16 to
32 (Jeff Thompson, personal communication).

Each field was annually rotated between corn and soybean crops, chisel plowed
in the fall and field cultivated in the spring prior to planting. The plots were
measured to ensure the same type of cultivar was planted in the same location as
in the previous soybean cropping year. The cropping timeline for the study is
shown in Table 1.

Table 1. Cropping timeline for SCN study in two fields at NWRC.

Field F4

Field E1

2001: R, MR, S soybean

2001: not used

2002: corn

2002: R, MR, S soybean

2003: R, MR, S soybean

2003: corn

2004: corn

2004: R, MR, S soybean

2005: S soybean only

2005: corn

2006: not used

2006: S soybean only

Field F4 in 2005 and field E1 in 2006 were planted 5 May 2005 and 10 May 2006, respectively, to the S cultivar Pioneer 92M91 in order to determine if the
effects of the previous cultivar choices could still be detected. Yields were
taken from the sites of individual plots corresponding to the respective
cultivars planted in the two previous soybean crops.

In 2001, field F4 had moderate SCN pressure of 890 SCN eggs/100 cm³
soil (stderr = 226) at planting. Field E1 in 2002 had an initial SCN population of
5888 SCN eggs/100 cm³ soil (stderr = 837) at planting. Population
densities of SCN were determined for each plot at planting and soybean maturity,
except in the final year when samples were collected at planting only. Soil
samples were a composite of eight 1 inch -diameter cores taken to a depth of ca.
8 inches from the middle 40 ft of the center two rows of each plot. The SCN
population density was quantified as number of eggs per 100 cm³ of soil by elutriation as described
previously (1,10).

Grain yield and moisture measurements were taken from combine harvest of the
center two rows of each plot. Plots were harvested 12 October 2001, 8 October 2002,
7 October 2003, 5 October 2004, 10 October 2005, and 20 September 2006. Yields were
corrected to 13% grain moisture. Data were analyzed with SAS (SAS Institute Inc.,
Cary, NC) procedures, including general linear models (GLM) and regression
(REG).

MR cultivars reduced the SCN population densities in both fields similarly to
the R cultivars, even though the initial population density was moderately high
in one field and relatively low in the other (Tables 2 and 3). The average
reduction in SCN population after two years with the moderately resistant
cultivars was slightly less than with the resistant cultivars, 2092 and 2923
eggs/100 cm³ soil, respectively, which were not significantly
different. This reduction contrasts with a significant increase (average of 4660
eggs) in SCN population after two years of planting SCN susceptible cultivars
(Table 2 and 3). There was an interaction between year and resistance (Pr > F =
0.001) for SCN population that was the result of higher number of eggs being
produced on the S cultivars for certain years.

Table 2. Effect of SCN resistance for 2 years on SCN population with
corn/soybean rotation.*

SCN cultivar
response category

SCN eggs/100
cm³ of soil from field F4, NWRC

Spring 01

Fall 01

Spring 03

Fall 03

Initial — Final
SCN

Resistant

1071

125

1118

207

-864

Moderately resistant

858

132

1162

603

-255

Susceptible

738

6007

6490

5847

5109

LSD 0.05

NS

4744

3895

2030

2133

* Data are the mean of two cultivars in each category.

Table 3. Effect of SCN resistance for 2 years on SCN population with
corn/soybean rotation.*

SCN cultivar
response
category

SCN eggs/100
cm³ of soil from field E1, NWRC

Spring 02

Fall 02

Spring 04

Fall 04

Initial — Final
SCN

Resistant

5903

2343

2540

920

-4983

Mod. resistant

6050

2437

1900

2120

-3930

Susceptible

5710

17325

6740

9920

4210

LSD 0.05

NS

3782

1703

3416

4226

* Data are the mean of two cultivars in each category.

In field F4, with a relatively low population of SCN (890 eggs) at the start
of the study, the resistant cultivars reduced the population 80%, almost below
the action threshold of 150 eggs (Table 2). The MR cultivar reduced the
population 30%, whereas the susceptible cultivars increased the SCN population
over six times higher to a moderately high level after only one year,
demonstrating how rapidly SCN can increase if not managed.

Results were similar in field E1, with the moderately high SCN population at
the beginning of the study (5888 eggs) (Table 3). The main difference in these
results from those from field F4 was in the amount by which the R and MR
cultivars reduced the population. The MR and R cultivars reduced the SCN
population 4000 to 5000 eggs from the initial population over two cropping
years, or 65 and 85%, respectively. Sixty percent of the reduction in SCN
numbers happened in the first year with both R and MR cultivars, with the R
cultivars causing further reduction the second year. As in field F4, the SCN
population in field E1 increased greatly with susceptible cultivars causing a
300% increase in SCN population the first year; with SCN numbers increasing the
second year to 170% higher than the initial egg counts.

These results show that cultivars labeled R and MR can have very similar
effects on the SCN population densities. Other subsets of cultivars from these
respective groups could be less similar in the degree they reduce SCN population
because of the FI of values assigned to each category. The criteria used to
determine if a cultivar is classified R or MR varies among seed companies, which
could include different FI values or relative yields in the presence of SCN.
Even with this standardized method of classifying varietal resistance to SCN,
there are still ranges for each group (6,8). Therefore, it should not always be
assumed that the SCN population will be reduced the same amount by resistant and
moderately resistant cultivars, as was the case in this study.

Moderately resistant cultivars consistently had the highest yields throughout
in this study (Table 4), averaging 27% greater than the yields of the
susceptible cultivars. The resistant cultivars averaged 19% greater yields than
the susceptible cultivars. The resistant cultivars tended to yield less than the
moderately resistant cultivars each year, although the difference was
significant only in 2004. There was no interaction between year and resistance
for yield (Pr > F = 0.38).

This study shows that soybean cultivars with moderate resistance to SCN can
be effective management tools for reducing SCN populations, much like cultivars
classified as resistant to SCN. While the R cultivars reduce the SCN population
more than MR cultivars, these differences were not significant in this study.
Placing the MR cultivars in most fields with SCN would be acceptable, although
it would be better to use R cultivars if the SCN populations are very high
(i.e., 7000 to 8000 eggs or more per 100 cm³). In such fields,
lowering the SCN population quickly is recommended, especially because our data
show that the yields of all cultivars are affected by SCN (Table 5).

Moderately resistant cultivars clearly have the potential to significantly
increase productivity of soybeans in a SCN infested field. The increased yield
potential seen with the MR cultivars over the R cultivars in this study suggests
that they would be a viable tool in managing SCN. Previously, there has been
reluctance by growers to plant SCN resistant cultivars because of the reported
yield drag. However, our data show that improvements in soybean genetics have
increased the yields of cultivars with moderate to high levels of resistance to
result in a yield benefit over high-yielding S cultivars even when the SCN
pressure is relatively low.

The yield comparison of MR and R cultivars in this study is between a very
small number of cultivars that are no longer sold by Pioneer Hi-Bred
International. However, comparing the top 20 yielding cultivars in University of
Illinois Region 2 Roundup Resistant cultivar trial in 2006, 16 were resistant to
HG 0, 2 moderately resistant and 2 susceptible in Maturity Group 2 (4,9) based
on Schmitt and Shannon’s differentiation of soybean cultivars. Similarly, in the
same trial with Maturity Group 3 cultivars, 12 of the 20 cultivars with the
highest yields were resistant, 7 moderately resistant, and 1 susceptible (labeled
resistant). This indicates that the genetics have improved yield potential of
SCN resistant soybean cultivars currently available, and that there is not the
yield drag once associated with all cultivars having resistance to SCN.

Bioassay of ‘Carry-over’ Effect from Previous Cultivars

The yield data from the S cultivar planted at the end of the study following
two years of soybeans that were resistant, moderately resistant or susceptible
to SCN showed there was a definite benefit of planting cultivars with some level
of SCN resistance that carries over to the next soybean crop (Table 6). The
yield of the S cultivar in the bioassay was 18% and 11% greater following the R
and MR cultivars, respectively, than following the susceptible cultivars. This
is primarily due to the reduced population density of SCN at planting (Fig. 1,
Table 6). The population density of SCN following two years with susceptible
cultivars was 3.8 and 9.7 times greater than following two years with MR and R
cultivars, respectively.

Fig. 1. The relationship between SCN population (eggs/100 cm³ of soil) at spring planting and yield of soybean. For less than10,000 eggs, this linear relationship is described by Y = 46.85 - 0.00259X (Pr > F = 0.0001, R² = 0.36). This bioassay was with SCN susceptible Pioneer 92M91 in 2005 and 2006 at NWRC.

Table 6. Effect of prior planting of SCN resistant cultivars for two crops on
yield and height of a susceptible soybean cultivar in corn/soybean rotation.*

SCN cultivar
in
previous
two crops

SCN population
at planting(eggs/100 cm³)

Soybean
bioassay
averages of 2005 and 2006

Height (inches)

Yield (bu/acre)

Resistant

625

33.6

44.3

Moderately resistant

1598

32.0

42.0

Susceptible

6093

29.4

37.7

LSD 0.05

2060

1.4

4.1

* Data are mean for cultivar Pioneer 92M91 planted in field F4 in 2005
and field E1 in 2006.

The data from the bioassay with the SCN susceptible cultivar (Fig. 1) showed
a negative relationship between the spring SCN egg counts and yield when the
population was less than10,000 eggs. This linear relationship is described by Y = 46.85 - 0.00259X (Pr > F = 0.0001, R² = 0.36). This means there was
2.6 bu/acre loss of yield for every increase of 1000 SCN eggs. Previous data from
NWRC has shown the yield loss per 1000 SCN eggs to range from 0.8 (Table 5) to
6.3 bu/acre (not shown). This range of yield loss can be related to the virulence
of the nematode and the environment (3) the first 60 days after planting, when
SCN are infecting the soybeans. In both years of the bioassay, the rainfall
totals during the growing seasons were very similar. As a result, in the
combined analysis of the two years of the bioassay, year was not a significant
factor (Pr > F = 0.23), nor was there an interaction of year with level of SCN
resistance (Pr > F = 0.29).

As the SCN population exceeds 10,000 eggs the relationship between population
and yield flattens out. The yield loss to SCN often levels off at the higher
populations, and even ultra-high levels of SCN will not kill soybeans
(T. L. Niblack,
personal communication). However, it is imperative to reduce the population of
SCN as quickly and as far as possible to be able grow soybeans profitably and to
help avoid the development of SCN populations virulent against current sources
of resistance to SCN.

Almost all of the Maturity Group 2 and 3 cultivars having SCN resistance are
from the same source, PI 88788, which creates concerns over cultivars losing
resistance after repeated cropping and selection of parasitic forms in the SCN
population. Therefore, it will be important to follow current recommendations to
not plant the same SCN resistant cultivars in the same field for consecutive
soybean crops. Even with the same source of resistance, the difference in the
package of resistance genes between cultivars will help avoid the same type of
intense selection pressure present when the same resistant variety is planted in
the same field. It was not a goal of this study to determine if there were
shifts in populations of SCN; however, it was determined that the population in
field E1 was HG Type 2.5.7 at the conclusion of the study (T. L. Niblack, personal
communication).

Incorporating Moderately Resistant Cultivars into SCN Management

This study shows the benefit of incorporating cultivars with some degree of
resistance to SCN to manage SCN, which includes those classified as moderately
resistant. Utilizing results from university cultivar trials in combination with
SCN resistance can reduce losses of yield to SCN and increase profit.
Furthermore, the benefit of SCN resistance carried over into the subsequent
planting of SCN-susceptible cultivars because of the reduction in SCN
populations. The improvements in genetics and information sources have given
growers the tools necessary to make good decisions to limit yield losses to SCN.

Acknowledgment

We thank Shelly Adee for her work on this paper. This study was funded in
part by Pioneer Hi-Bred International.